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Phylogenetic Relationships of the Gomphales Based on Nuc-25S-Rdna, Mit-12S-Rdna, and Mit-Atp6-DNA Combined Sequences

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Phylogenetic Relationships of the Gomphales Based on Nuc-25S-Rdna, Mit-12S-Rdna, and Mit-Atp6-DNA Combined Sequences Phylogenetic relationships of the Gomphales based on nuc-25S-rDNA, mit-12S-rDNA, and mit-atp6-DNA combined sequences a b Admir J. GIACHINl ,*, Kentaro HOSAKA , Eduardo NOUHRAc, d A Joseph SPATAFORA , James M. TRAPPE ARTICLE INFO ABSTRACT Phylogenetic relationships among Geastrales, Gomphales, Hysterangiales, and Phallales were estimated via combined sequences: nuclear large subunit ribosomal DNA (nuc-25S- rDNA), mitochondrial small subunit ribosomal DNA (mit-12S-rDNA), and mitochondrial atp6 DNA (mit-atp6-DNA). Eighty-one taxa comprising 19 genera and 58 species were inves- tigated, including members of the Clathraceae, Gautieriaceae, Geastraceae, Gomphaceae, Hysterangiaceae, Phallaceae, Protophallaceae, and Sphaerobolaceae. Although some nodes Keywords: deep in the tree could not be fully resolved, some well-supported lineages were recovered, atp6 and the interrelationships among Gloeocantharellus, Gomphus, Phaeoclavulina, and Turbinel- Gomphales Ius, and the placement of Ramaria are better understood. Both Gomphus sensu lato and Rama- Homobasidiomycetes ria sensu lato comprise paraphyletic lineages within the Gomphaceae. Relationships of the rDNA subgenera of Ramaria sensu lato to each other and to other members of the Gomphales were Systematics clarified. Within Gomphus sensu lato, Gomphus sensu stricto, Turbinellus, Gloeocantharellus and Phaeoclavulina are separated by the presence/absence of clamp connections, spore orna- mentation (echinulate, verrucose, subreticulate or reticulate), and basidiomal morphology (fan-shaped, funnel-shaped or ramarioid). Gautieria, a sequestrate genus in theGautieria- ceae, was recovered as monophyletic and nested with members of Ramaria subgenus Ramaria. This agrees with previous observations of traits shared by these two ectomycor- rhizal taxa, such as the presence of fungal mats in the soil. Clavariadelphus was recovered as a sister group to Beenakia, Kavinia, and Lentaria. The results reaffirm relationships be- tween the Geastrales, Gomphales, Hysterangiales, and the Phallales, suggesting extensive convergence in basidiomal morphology among members of these groups. A more extensive sampling that focuses on other loci (protein-coding genes have been shown to be phyloge- netically informative) may be useful to answer questions about evolutionary relationships among these fungal groups. © 2010 The British Mycological Society. Published by Elsevier Ltd. All rights reserved. (1954), Heinemann (1958), Donk (1964),Giachini (2004) and Introduction Hosaka et al. (2006), Clavariadelphus is a member of the Gom- phales. The results of Villegas et al. (1999), however, disagree The gomphoid fungi occupy a unique position in the phylog- with the premises that ClavarIadelphus, Gomphus, and Ramaria eny of higher Basidiomycetes (Bruns et al. 1998; Pine et al. are members of the same order. According to those authors 1999; Hibbett & Thorn 2001; Hosaka et al. 2006). They are prom- Clavariadelphus is not grouped within but rather a sister group inent in most forest ecosystems as saprotrophs and mutual- to the Gomphales. ists. The fungi in this group are also characterized by a wide Pine et al. (1999) and Humpert et al. (2001), on the other range of basidiomal morphologies, from stalked ramarioid/ hand, using sequences of both mitochondrial (mit-12S- clavarioid to cantharelloid-gomphoid, clavate, resupinate- rDNA) and nuclear (nuc-25S-rDNA) loci, showed that a gom- odontoid, to sequestrate. Molecular studies reveal that gom- phoid-phalloid clade including Clavariadelphus, Geastrum, phoid fungi are closely related to taxa in the Geastrales, Hys- Gloeocantharellus, Gomphus (monophyletic), Lentaria, Ramaria terangiales, and Phallales (Colgan et al. 1997; Hibbett et al. (paraphyletic), Pseudocolus, and Sphaerobolus was recovered 1997; Pine et al. 1999; Humpert et al. 2001; Hosaka et al. 2006). in all analyses performed. Pine et al. (1999) showed that Gom- Taxonomy of the Gomphales has traditionally relied upon phus sensu lAto represented a terminal monophyletic group in morphological characters now known to be subject to parallel the gomphoid-phalloid clade (although just two taxa were evolution and phenotypic plasticity (Moncalvo et al. 2000). sampled), having Ramaria as sister group (Figs 1-3 in Pine Consequently, many current genera and families are artificial, et al. 1999). Based on morphological as well as molecular and taxonomic limits and identity of natural groups in the or- characters, Giachini (2004) revisited the generic concepts in ders Geastrales, Gomphales, Hysterangiales, and Phallales are the family Gomphaceae and recombined the species being re-examined. of Gomphus sensu lato into Gloeocantharellus, Gomphus Past workers (Maire 1902, 1914; Eriksson 1954; Heim 1954) sensu stricto, and the resurrected genera Phaeoclavulina and recognized the relatedness of diverse morphologies within TurbInellus. the Gomphales from microscopic and macrochemical charac- Cantharelloid/gomphoid and clavarioid fungi have his- ters, including cyanophilic spore ornamentation, chiastic torically been prominent in hypotheses about the origin of basidia, hyphal construction, and positive hymenial reaction fleshy basidiomycetes (Singer 1947, 1986; Heim 1954; to ferric sulfate (Eriksson 1954; Donk 1961, 1964; Petersen Corner 1966;Harrison 1971; Petersen 1971a; Corner 1972; 1971a; Villegas et al. 1999).Donk (1961,1964)proposed the fam- julich 1981; Miller & Watling 1987). Their fruiting forms can ily Gomphaceae to include the resupinate-odontoid genera be arranged in a transformation series, from clavate at one Kavinia and RamarIcium, the stalked clavarioid-ramarioid gen- end, cantharelloid/gomphoid intermediately, and agaricoid era Lentaria and Ramaria, the stalked hydnoid genus Beenakia, at the other extreme. Corner (1972) proposed the "Clava ria the stipitate agaricoid genus Gloeocantharellus, and the pile ate theory" of basidiomycete evolution in which cantharelloid genera Chloroneuron and Gomphus. Corner (1970) proposed and clavarioid fungi were to be regarded as ancestral, and Ramariaceae to include Delentaria, Kavinia, LentarIa, and Rama- from which all other Homobasidiomycetes have been de- ria. He excluded the pileate genera because no intermediate rived. He suggested that simple clavate morphologies (e.g. species linked the gomphoid and ramarioid morphologies. Clavaria) with smooth hymenia gave rise to intermediate Petersen (1971a) suggested a gomphoid ancestral morphology cantharelloid species (e.g. CantHarellus, Craterellus), and for the family and later revised Donk's and Corner's familial from those were derived the wrinkled or folded hymenial classifications to include Beenakia, GompHus, KavinIa, RamarI- gomphoid species (e.g. Gomphus, Turbinellus). Other authors cium, Ramariopsis, and RamarIA (Petersen 1973, 1988). agree on transformations among ramarioid, cantharelloid, Morphological and recent molecular data (mitochondrial and agaricoid forms but propose the opposite polarity, sug- and nuclear rONA) have been used to infer inter- and intra- gesting that lineages containing cantharelloid, ramarioid, specific relationships among genera in this group of fungi. and club-like fungi have been derived from agaricoid ances- According to Pine et al. (1999), Villegas et al. (1999), Humpert tors (Fiasson et al. 1970; Arpin & Fiasson 1971; Petersen et al. (2001), and Hosaka et al. (2006), the Gomphales includes 1971a; Singer 1986). the genera Beenakia, Clavariadelphus, Gautieria, Gloeocantharel- In this paper we analyze phylogenetic relationships among Ius, Gomphus, KavInia, Lentaria, Phaeoclavulina, RamarIa, RamarI- major evolutionary lineages of gomphoid fungi using com- cium, and Turbinellus. Hosaka et al. (2006) demonstrated the bined sequence data from nuclear (nuc-25S-rDNA) and Gomphales to be a sister group to the Phallales, represented mitochondrial-encoded ribosomal and non-ribosomal RNA by the families Clathraceae (sensu Chevallier), Phallaceae genes (mit-12S-rDNA, mit-atp6-DNA). Our taxonomic sam- (sensu Corda), Lysuraceae, Protophallaceae (sensu Zeller), pling focused on the Gomphales sensu Julich (1981). Major Claustulaceae, and Trappeaceae. Both Gomphales and Phal- questions tested in this study were: lales are closely related to the Hysterangiales (sensu Hosaka & Castellano) and the Geastrales. 1) Is Gomphus sensu lato monophyletic? Villegas et al. (1999), using morphological traits, proposed 2) Are genera within Gomphus sensu lato monophyletic? the Gomphales to be monophyletic and delimited by the pres- 3) Are the Gomphales, Hysterangiales, Phallales, and Geas- ence of mycelial cords or rhizomorphs. It included the families trales closely related? Beenakiaceae (Beenakia, KavinIa, and RamaricIum), Gompha- 4) How have basidiomatal morphology, presence or absence ceae (Gomphus and Gloeocantharellus), Lentariaceae (Lentaria), of clamp connections, and substrate affinity evolved and Ramariaceae (RamarIA). According to Singer (1949), Heim within the Gomphales? the Kishino-Hasegawa (K-H)test implementing the likelihood Materials and methods model described above (Table 2). Character state reconstruc- tion for substrate affinity, basidiomata morphology, and pres- TaxonomiC samplinG ence/absence of clamp connections was performed in Mr 3 Bayes (MC ) version 3.0 (Huelsenbeck & Ronquist 2001); equal The sampling of Geastrales, Gomphales, Hysterangiales, and weights for all character state transformations were assumed. Phallales included 19 genera and 58 species (total of 81 taxa) as listed along with GenBank
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